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Ann Thorac Surg 2003;75:82-87
© 2003 The Society of Thoracic Surgeons

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Original article: cardiovascular

Nonthyroidal illness syndrome in off-pump coronary artery bypass grafting

^a Unità Operativa di Cardiochirurgia Adulti, Massa, Italy
^b Unità di Endocrinologia Cardiovascolare, Ospedale "G. Pasquinucci," Massa, Italy

Accepted for publication June 17, 2002.

* Address reprint requests to Dr Cerillo, U. O. Cardiochirurgia Adulti, Ospedale "G. Pasquinucci," Via Aurelia Sud, 54100 Massa, Italy.
e-mail: cerillo{at}ifc.cnr.it

	Abstract

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BACKGROUND: Cardiopulmonary bypass (CPB) is an established cause of nonthyroidal illness syndrome (NTIS). Off-pump coronary artery bypass (OPCAB) has been reported to be less invasive than coronary artery bypass grafting (CABG) with CPB. We prospectively evaluated thyroid metabolism in OPCAB patients.

METHODS: We analyzed free thyroid hormones (FT3 and FT4), thyroid-stimulating hormone (TSH), and reverse T3 (rT3) in 20 consecutive patients undergoing CABG surgery. Nine patients underwent CABG with CPB, and 11 underwent OPCAB. Blood samples were taken on admission, on the day of surgery (7:30 AM), after sternotomy, at the end of the operation, and at 2, 6, 12, 24, 36, 48, 72, 96, 120, and 144 hours postoperatively. The concentrations of FT3, FT4, and TSH were determined on each sample. Reverse T3 concentration was measured in 10 patients up to 48 hours and at 144 hours postoperatively.

RESULTS: Baseline, operative, and postoperative variables were similar in the two groups. FT3 concentration dropped significantly (p < 0.0001), reaching its lowest value 12 hours postoperatively. There were no significant differences between CPB and OPCAB patients. FT4 varied significantly in both groups (p < 0.0001), but remained in the normal range. TSH variation was not significant. rT3 concentration rose significantly (p = 0.0002) in both groups, peaking 24 hours after surgery.

CONCLUSIONS: OPCAB induces a NTIS similar to that observed after CPB, probably due to the inhibition of T4 conversion to T3. This finding suggests that NTIS is a nonspecific response to stress. CPB should not be considered as the sole trigger of NTIS in cardiac surgical patients.

	Introduction

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The "nonthyroidal illness syndrome" (NTIS), also referred to as the "euthyroid sick syndrome" [1], is a spectrum of hypothalamus-pituitary-thyroid axis dysfunction ranging from a mild form, characterized by isolated low triiodothyronine (T3) levels, to a more complex syndrome associated with low T3 and low thyroxine (T4) levels [2]. NTIS has been observed in starvation, sepsis, myocardial infarction, cardiac and noncardiac surgery, and is probably present in any severe illness [2, 3]. Cardiopulmonary bypass (CPB) is an established cause of NTIS, and the peculiar changes in the cardio-circulatory physiology that it brings about (hemodilution, nonpulsatile flow, systemic heparinization, hypothermia) have been implicated as a possible cause of this condition [4–6].

With the introduction of effective devices for heart stabilization and the refinement of cardiac anesthesia, off–pump coronary artery bypass grafting (OPCAB) is gradually establishing its position in practice, and is currently considered an adequate therapeutic option for patients with multivessel coronary artery disease [7, 8]. OPCAB offers several advantages in comparison with on-pump myocardial revascularization, in terms of myocardial protection [9, 10], neurocognitive outcome [11], and inflammatory response [12]. To the best of our knowledge, previous reports on cardiac surgery–related NTIS have been focused on patients operated on CPB. To assess whether OPCAB reduces postoperative T3 deficiency, we prospectively analyzed 20 patients undergoing elective surgical myocardial revascularization with or without CPB.

	Material and methods

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Patients
Thirty-nine consecutive patients undergoing surgical myocardial revascularization at our institution during July 2001 were assessed for eligibility. Exclusion criteria included history of thyroid disease, preoperative therapy with drugs known to interfere with thyroid function [13], surgical procedures other than CABG, perioperative blood product transfusions, severe systemic illness, relevant renal or hepatic dysfunction, and urgent and emergency procedures.

Eleven patients undergoing OPCAB (OPCAB group) and 9 patients undergoing CABG with CPB (CPB group) were finally included.

This study was approved by the Ethical Committee of the "G. Pasquinucci Hospital" and the "Institute of Clinical Physiology" of the Italian National Research Council. Written informed consent was obtained from all patients.

Blood sampling
Blood samples were taken on hospital admission, on the day of surgery (7:30 AM), after sternotomy, at the end of the surgical procedure, and then at 2, 6, 12, 24, 36, 48, 72, 96, 120, and 144 hours postoperatively. Each blood sample was stored at 4°C and centrifuged within 6 hours. Free-triiodothyronine (FT3), free-thyroxine (FT4), and thyroid-stimulating ormone (TSH) concentrations were measured on each sample. Short-term analysis of reverse T3 (rT3) concentration was carried out in 5 CPB and 5 OPCAB patients (from the day of surgery until 48 hours after surgery). Reverse T3 was also measured in these patients at 144 hours.

Assay methods
Serum FT4, FT3, and TSH concentrations were measured by the fully automated AIA 1200 System Analyzer (TOSOH Corporation, Tokyo, Japan). To minimize assay errors, all serum samples from the same patient were assayed at the same time. The sensitivity and intraassay precision of these methods have been previously reported [14].

Serum rT3 concentrations were determined in triplicate using a commercially available radio immunoassay kit (BioChem Immunosystems, Bologna, Italy).

Perioperative and surgical management
On the night before the operation, all patients received 4 mg of oral Diazepam. Premedication (Morphine 0.1 mg/kg and Scopolamine 0.25 to 0.4 mg) was administered IM on the day of surgery, 30 to 45 minutes before patient transferral to the operating theater. Intravenous anesthesia was inducted with Diazepam 0.2 mg/kg, Fentanyl 2 to 4 µg/kg, and Pancuronium 0.1 mg/kg, and maintained by boluses of Fentanyl (up to a total dose of 12 to 20 µg/kg) and Pancuronium (0.04 mg/kg every 45 to 60 minutes) combined with a continuous infusion of Propofol (3 to 5 mg/kg/h). Before skin incision, all patients received an antibiotic prophylaxis with Cefuroxim (2,000 mg).

Heparin dosage was 300 IU/kg for patients undergoing CPB, and 200 IU/kg in off-pump procedures. Patients undergoing CPB routinely received a bolus of methil-prednisolone (20 mg/kg IV) and a bolus of tranexamic acid (50 to 100 mg/kg IV) intraoperatively. CPB was conducted with ascending aorta and two-stage right atrium cannulation. Hyperkalemic warm-blood cardioplegia was administered every 10 to 15 minutes through the aortic root. The pump circuit was primed with a balanced solution (Ringer’s lactate 1,000 mL, Hydroxy-ethyl starch 500 mL, mannitol 250 mL, NaHCO₃ 60 mEq, heparin 100 mg). Flow was maintained at 2.4 to 2.8 L/min/m² with moderate hypothermia (34°C). A standard nonheparinized circuit (Dideco SpA, Mirandola, Italy) and membrane oxygenator (Monolyth-Oxygenator Sorin-Biomedica Cardio, Saluggia, VC, Italy) were used.

In the OPCAB group, a commercially available stabilization device (Octopus Medtronic; Medtronic Inc, Minneapolis, MN) achieved exposure and immobilization of the diseased vessels. Two silastic snares obtained temporary control of blood flow during the anastomoses. An intravascular shunt was used to reduce the ischemic period and to minimize bleeding in the surgical field. The proximal anastomoses of vein grafts were performed during lateral aortic clamping, before the distal anastomoses.

Postoperative morbidity
Hospital mortality was defined as any death occurring before hospital discharge or within 30 days after surgery. Transient ischemic attack (TIA) was defined as a completely reversible neurologic deficit lasting less than 24 hours. Perioperative myocardial infarction was defined as the presence of two or more of the following criteria: enzymatic elevation (CK-MB > 10% of total CK or Troponine I > 0.5 ng/mL), new Q waves greater than 0.03 ms or a reduction in R waves greater than 25% in two leads, and new akinetic segment(s) shown at echocardiogram. Low-output syndrome was defined as the need of inotropic support (IABP or drugs, or both, for more than 12 hours). Acute renal failure was defined as a postoperative creatinine more than 2 mg/dL with a serum creatinine rise 0.7 mg/dL versus baseline. Acute respiratory failure was defined as the need of mechanical ventilation for more than 24 hours or the need of reintubation.

Cardiorespiratory rehabilitation was counted in the postoperative stay, and patients were considered discharged only when they went home.

Statistical analysis
Continuous variables are expressed as means ± standard deviation. Dichotomous variables are expressed as percentages. Dichotomous variables were analyzed by the Pearson ² test or, where appropriate, by Fisher’s exact test. Continuous variables were analyzed by unpaired Student’s t test. Longitudinal data, including hormone concentrations, were analyzed by the analysis of variance for repeated measurements. The Bonferroni test was used for posthoc multiple comparisons. Analyses were performed using Statview 5.0 (SAS Institute Inc, Cary, NC). A p value 0.05 was considered significant.

	Results

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Baseline and operative variables
Patient baseline and operative characteristics are shown in Table 1. Seven patients (63.6%) in the OPCAB group had two-vessel disease, whereas all patients in the CPB group had three-vessel disease (p = 0.004). As a consequence, CPB patients received an average of 3.5 bypass grafts, whereas off-pump patients received 2.4 bypass grafts (p = 0.0004). Despite this difference, a complete myocardial revascularization was achieved in all patients. No other significant differences were found between the two groups.

Mean postoperative intensive care unit stay was 26.4 ± 17.7 hours. Mean postoperative stay was 13.4 ± 3.8 days.

Hormonal profile
FT3 was in the normal range (2.1 to 4.2 pg/mL) in all patients at admission (2.5 ± 0.35 pg/mL). After an initial peak at sternotomy (2.8 ± 0.5 pg/mL, p = 0.09 vs baseline), FT3 concentration dropped significantly, reaching its lowest value 12 hours after surgery (1.5 ± 0.5 pg/mL, p < 0.0001 vs base line), and then slowly returned to normal values by postoperative day 6 (2.1 ± 0.6 pg/mL; Fig 1). FT3 varied similarly in CPB and OPCAB patients (p = 0.67).

View larger version (25K): [in this window] [in a new window]   Fig 1. Mean ± SE FT3 concentrations in CPB and OPCAB patients. Sampling times are as follows: A = at admission; M = on the morning of the operation; S = at sternotomy; F = at the end of surgery; t2-t144 = at 2 to 144 hours postoperatively. Circles = CPB; squares = OPCAB.

View larger version (29K): [in this window] [in a new window]   Fig 2. Effect of amiodarone therapy on postoperative FT3 concentrations. Mean ± SE postoperative FT3 concentrations were similar in treated (circles) and untreated (squares) patients at each time point. The Bonferroni test was not significant (p = 0.61). Sampling times are as follows: A = at admission; M = on the morning of the operation; S = at sternotomy; F = at the end of surgery; t2-t144 = at 2 to 144 hours postoperatively. Circles = yes; squares = no.

View larger version (31K): [in this window] [in a new window]   Fig 3. Mean ± SE FT4 concentrations in CPB and OPCAB patients. Sampling times are as follows: a = at admission; m = on the morning of the operation; s = at sternotomy; f = at the end of surgery; t2-t144 = at 2 to 144 hours postoperatively. Circles = CPB; squares = OPCAB.

View larger version (28K): [in this window] [in a new window]   Fig 4. Mean ± SE TSH concentrations in CPB and OPCAB patients. Sampling times are as follows: A = at admission; M = on the morning of the operation; S = at sternotomy; F = at the end of surgery; t2-t144 = at 2 to 144 hours postoperatively. Circles = CPB; squares = OPCAB.

View larger version (25K): [in this window] [in a new window]   Fig 5. Mean ± SE rT3 concentrations in CPB and OPCAB patients. Circles = CPB; squares = OPCAB. Sampling times are as follows: A = at admission; M = on the morning of the operation; S = at sternotomy; F = at the end of surgery; t2-t144 = at 2 to 144 hours postoperatively.

	Comment

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Previous reports on NTIS in cardiac surgical patients presented some limitations that still need to be addressed. To the best of our knowledge, all previous studies have focused on patients operated on CPB, leading to the misconception that CPB is the cause of NTIS during and after cardiac surgery [1, 4, 6, 7, 16, 17]. Our results indicate that this hypothesis should be reconsidered. Previous research investigated the effect of different CPB techniques on the thyroid metabolism. A prospective study by Thrush and coworkers [5] revealed no differences in total T3, total T4, FT3, rT3, and TSH concentrations in two group of patients undergoing either normothermic or hypothermic CPB, showing that normothermia does not prevent the onset of NTIS. In light of our results, this is not surprising. A better thyroid function has been reported instead in patients undergoing CPB with pulsatile perfusion [4, 6]. In a recent report [6], Silistreli and coworkers found total T3 and FT3 levels "closer to normal" in patients undergoing pulsatile perfusion in comparison with patient undergoing nonpulsatile perfusion, and concluded that this "may result in a potential positive inotropic effect." However, the levels of FT3 were similar in the two groups both after 60 minutes of perfusion and 24 hours postoperatively. Furthermore, the lower FT3 concentration they reported (30 minutes after the onset of CPB, in the pulsatile perfusion group) was more than 2 pg/mL. This strongly argues against a possible beneficial effect of the pulsatile perfusion on thyroid metabolism.

Another point needs attention. Many previous reports were limited to the intraoperative and early postoperative period [1, 6, 16]. In our series, the maximal degree of thyroid metabolism derangement was observed 12 hours after the end of the operation, and FT3 concentration was still below the normal value by postoperative day 5. Furthermore, rT3 peak concentration was observed 24 hours after surgery, and rT3 was still elevated by postoperative day 6. These findings are consistent with previous observations [5, 17], and should be taken into account when considering the opportunity of a substitutive therapy with exogenous T3 [5].

The finding that OPCAB induces thyroid metabolism alterations similar to that observed after CPB is not unexpected, because NTIS is known to occur in a wide spectrum of conditions, including starvation, sepsis, severe illness, and surgery [2, 3]. In this view, NTIS may be regarded as an aspecific adaptive mechanism with a common pathophysiology, that is, the inhibition of the peripheral conversion pathway of T4 to T3 (decreased 5'-mono-deiodinase activity).

Some limitations of the present study need to be addressed. Although this was a prospective study, patients were not randomly assigned to the CPB or OPCAB group. The decision to use CPB or not was left to the operating surgeon, and most often based on the quality and extension of disease of the target vessels. As a result, the number of the diseased vessels and the average number of bypass grafts were less in the OPCAB group. This notwithstanding, all patients in both groups received a complete myocardial revascularization, and no complications referable to myocardial ischemia were observed. Furthermore, one could expect patients with a less diseased coronary circulation, undergoing less invasive operations, to exhibit a less marked alteration of the thyroid metabolism, and this was not the case. It is noteworthy that the operative time, the postoperative intensive care unit length of stay, and the duration of postoperative mechanical ventilation were similar in the two groups (Tables 1, 2). This may have resulted in a similar postoperative thyroid metabolism. For these reasons, we believe that our research was not invalidated by selection bias.

Another possible source of bias is represented by the fact that the massive hemodilution that occurs in patients undergoing CPB is not expected to occur in OPCAB patients. As a result, total thyroid hormone concentrations may be falsely low in CPB patients. For this reason, we decided to assay the biologically active, free-thyroid hormone fraction. In fact, it has been proven that the measurement of FT4 and FT3 concentration is not affected by hemodilution [18].

Several previous studies have shown that NTIS in cardiac surgical patients does not merely represent a dilutional effect, and that it is associated with low thyroid hormone availability to tissues [1, 2, 5, 17]. Hypothyroidism is associated with increased systemic vascular resistance, decreased heart rate, decreased cardiac output, and prolonged isovolumic relaxation time [19]. All these factors are known to negatively affect the postoperative course in cardiac surgery. Based on the assumption that cardiac surgery–related NTIS may worsen postoperative cardiac performance, T3 has been introduced in the management of cardiac surgical patients, with some encouraging results [20–23]. Our data show that surgical myocardial revascularization induces a marked and prolonged alteration of the thyroid metabolism, and that off-pump surgery does not improve the perioperative thyroid function. However, this study does not address the question of whether patients with NTIS are actually hypothyroid, and whether a substitutive therapy should be undertaken. Large, prospective trials are probably needed to identify clinical or laboratory measurements able to discriminate which patient may actually benefit from substitutive therapy and which may not.

	Acknowledgments

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We wish to acknowledge Samira Volpi, Susan Gwynne, and Elaine Laws for their expert assistance in manuscript preparation.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Pier Andrea Farneti Mattia Glauber Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Cerillo, A. G. Articles by Glauber, M. Search for Related Content PubMed PubMed Citation Articles by Cerillo, A. G. Articles by Glauber, M. Related Collections Minimally invasive surgery